Background: Alopecia areata (AA) is a common, chronic inflammatory disease characterized by nonscarring hair loss on the scalp or any hair-bearing area of the body. Recently, dermoscopy, a noninvasive diagnostic procedure, has been employed for the diagnosis of AA. Aim: To evaluate various dermoscopic patterns in AA and correlate these patterns with the disease activity and severity. Materials and Methods: Dermoscopy was performed on AA patients using DL1 dermoscope (magnification ×10 was used). The dermoscopic patterns recorded were analyzed to identify any correlation with the disease activity and severity. Results: A total of fifty patients of AA were recruited in the study. Female outnumbered males with the ratio being 1.173:1. Mean age of the patients was 25.06 years. Mean duration of disease was 14 months. The most common site involved was scalp (80%) and type noted was patchy (84%). Various dermoscopic patterns noted were yellow dots (YD) (88%), short vellus hair (66%), black dots (BD) (58%), broken hairs (BHs) (56%), tapering hair (TH) (26%), Coudability hairs (14%), pigtail hair (14%), and Pohl-Pinkus constrictions (2%). Statistically significant correlation was observed between BD, BHs, THs, and disease activity. No significant correlation was found between severity and any of the dermoscopic features. Conclusion: The most common dermoscopic pattern in our study was YD. Presence of BDs, BHs, and THs indicate active disease. Dermoscopic patterns were not affected by severity of the disease.

Alopecia areata (AA) is a common, chronic inflammatory disease characterized by nonscarring hair loss on the scalp or any hair-bearing area of the body. It accounts for 25% of all alopecia cases presenting to the dermatologists and 2-3% of all new outpatient dermatology services in the USA and the UK, 3.8% in China, and 0.7% in India. [1],[2],[3],[4] Although AA may occur at any age, incidence is high among younger age group; in fact, it is the most common form of alopecia seen in children. Various patterns of alopecia described clinically are patchy, diffuse, reticulate, ophiasis, ophiasis inversus, and depending on the extent of hair loss, alopecia subtotalis, alopecia totalis (complete loss of scalp hair), and alopecia universalis (complete loss of body hair) are described. [5]

AA is diagnosed clinically by the presence of well-circumscribed, round, or oval bald patches with smooth surface and characteristic exclamation mark hair. In the past, doubtful cases were confirmed by invasive procedures such as punch biopsy, which at times can be troublesome in pediatric age group. This problem has been overcome by dermoscopy, a noninvasive diagnostic procedure, which magnifies subtle clinical surface features of skin lesions as well as unveils some subsurface skin structures normally not visible even with a magnifying lens. [6] Various dermoscopic features in AA that are already described in the literature are black dots (BD) (cadaverous hairs), yellow dots (YD), tapering hairs (THs) (exclamation mark hairs), broken hairs (BHs), etc. [7] With this background, we conducted a study to evaluate various dermoscopic patterns in AA that help in diagnosis and to correlate these patterns with disease activity and severity so that ideal treatment can be planned.

Materials and Methods

We conducted a cross-sectional study on all AA patients attending to the outpatient department of our hospital from January 2013 to September 2014 after obtaining Institutional Ethical Committee clearance. All the patients with AA irrespective of age and sex who were willing to undergo the protocol were included in the study. An informed consent was obtained from the patient or parent or guardian in case of a child. Cases of AA were clinically diagnosed, and biopsy was done in ambiguous cases. Epidemiological data (name, age, sex, and occupation), relevant history (age of onset, duration of the disease, history of atopy, association with other autoimmune diseases, and family history), and clinical examination including general, systemic, and cutaneous examinations were documented. Biopsy was done in two cases to confirm the diagnosis. A number of patches, distribution, pattern, morphology, and characteristic features if any were noted.

Dermoscopic patterns of the patches were noted with the help of DL1 dermoscope (DermLite, 3 Gen LLC, San Juan Capistrano, CA, USA) (magnification × 10) that can be used without immersion oil because of the presence of polarized filters. Dermoscope was attached to Samsung Galaxy S3 smartphone with an adaptor [Figure 1] and [Figure 2]. Dermoscopic features were observed, and the photographs were taken with the help of camera of mobile device. Later, they were transferred to the laptop and were stored for further comparison and analysis. Assessment of disease activity was based on the subjective history of progression and an objective evaluation of hair pull test at the margins of each individual patch. Severity of disease was assessed by severity of alopecia tool (SALT) score calculated based on the combination of extent and severity of scalp hair loss. The dermoscopic patterns recorded were analyzed to identify a correlation between any of the specific dermoscopic features and the disease activity and severity by Spearman rank-order correlation coefficient by rank test and their statistically significant was determined by calculating P value.

Fifty patients of AA were recruited in the study. Most of the patients (86%) were younger than 40 years. There was an extreme variation in the duration of the disease, ranging from 10 days to 8 years. The alopecia remained confined to the scalp in 72% (36/50) of the cases, only body hair was involved in 20% (10/50), and both were involved in 8% (4/50) of the cases. Most common type of AA in our study was patch type. Localized patches (1-3) were seen in 70% (35/50) of the cases and multiple patches (>3 patches) were seen in 14% (7/50) of the cases. Demographic and clinical details were given in [Table 1]. In the present study of fifty patients, there were a total of 109 patches and hair pull test was done at the margins of each individual patch to assess the activity. It was positive in 35% (38) of the patches and negative in 65% (71) of the patches. Grade S1 severity was found in 58% of the study population as determined by SALT score, the details were represented in [Figure 3].

Dermoscopic evaluation of the scalp in the current study revealed different hair shaft abnormalities and various patterns at hair follicle openings against the background of honeycomb pigment network. The most common finding was YDs followed by short vellus hair (SVH) [Table 2] and [Figure 4][Figure 5][Figure 6][Figure 7][Figure 8][Figure 9]. Micro-exclamation mark hair was seen in 16% (8/50) of the cases. Statistically significant correlation was observed between BD, BHs, TH, and disease activity. SVHs correlated negatively with the disease activity, but this was not statistically significant [Table 3]. No significant correlation was found between the severity and any of the dermoscopic features [Table 4].

Dermoscopy has been established as an essential tool in the diagnosis of various hair disorders. Lacarrubba et al. [8] first described videodermoscopic features of AA in 2004. Since then, it was widely used in this field because of its ease and noninvasiveness.

[Table 2] depicts the comparison of dermoscopic features of our study with other Indian studies and with the study done in Japan.

Yellow dots

They represent distended follicular orifices of the affected follicles, filled with sebum and keratinous material. They appear as round or polycyclic, yellow to yellow-pink dots devoid of hairs or contain miniaturized or cadaverized or dystrophic hairs. In our study, YDs were seen in 88% (44/50) of cases, similar to the other studies. [9],[10],[11] However, some studies reported lesser incidence. [7],[12],[13] This variation in results can be attributed to the difference in skin types (yellowish color of skin in Asians may make it difficult to perceive the YDs on dermoscopy), different shampooing habits, and difference in the type of dermoscope used. [7],[14] In view of their higher frequency in AA as reported by various studies including ours, YD can be regarded as a sensitive marker for the diagnosis of AA.

Black dots (cadaverous hairs)

They are the remnants of BH and TH. BD is difficult to appreciate in Caucasians due to the hair color. In our study, BD was seen in 58% of the cases, and the result was comparable to that of Karadag Köse and Güleç [11] and Mane et al.[10]

Broken hairs

BH results either from the transverse fracture of terminal hair shafts weakened by the inflammatory process or by rapid regrowth of incompletely destroyed hair shafts that previously formed the BDs. They are not specific to AA as they are also seen in other conditions such as trichotillomania. In AA, usually hairs are broken at the same level above the skin surface, whereas in trichotillomania, every BH has a different length. [15] In our study, BH was seen in 56% of the cases on par with Mane et al.[10] study. Some studies reported lesser incidence. [7],[11],[12] These variations in results may be due to difference in activity, severity, and duration of the disease in various studies. [15]

Tapering hairs (exclamation mark hairs)

They represent fractured hairs with frayed thicker distal end and thinner proximal shaft. Clinically visible TH is of approximately 1 cm long, whereas dermoscopy aids in visualizing exclamation mark hairs of even 1-2 mm long, the latter are referred to as "micro-exclamation mark hairs." On clinical examination, TH was seen in only 5 (10%) cases but with dermoscopy they (micro-exclamation mark hairs) were found in additional 8 (16%) cases (total of 13 patients [26%]). Thus, dermoscopy was more sensitive in picking up TH than the naked eye and as this finding indicates active disease, [7] ideal treatment plan can be tailored. Studies of Inui et al.[7] and Peter et al. [13] reported slightly higher incidences of TH.

Coudability hairs

They were initially described by Shuster in 1984, as normal looking hairs that can be made to kink easily when bent or pushed inward. [16] An interesting hypothesis was that coudability hairs (CH) precede BD and TH, as it appears in seemingly intact hairs of normal length. They were seen in 14% of cases in the present study, compared to 12-42% reported by Rudnicka et al. [15]

Short vellus hairs and pigtail hairs

Lacarrubba et al. [8] described two patterns of hair regrowth in some patients with chronic AA, one was homogeneous and <10 mm long hair indicating early disease remission (upright vellus hair) and second was sparse, thin and twisted vellus hair with characteristic circular hair pattern pigtail hair (PTH) that were usually lost after few weeks. Regrowth of SVH after treatment can be seen in dermoscopy even before they can be perceived by the naked eye. In the present study, SVH was seen in 66% of the patients, similar to Hegde et al. [12] study. Peter et al.,[13] and Mane etal.[10] found a lower incidence of SVH. This variation in the incidences may be attributed to the difference in exposure of patients to various treatment modalities before being included in the study. PTH was seen in 14% of the patients in the current study, whereas Peter et al.[13] reported it in 17.5% of the patients. As there were very few studies reporting PTH incidence, further studies with large sample size and follow-up are necessary to comment on its evolution and prognostic significance.

Pohl-Pinkus constrictions

They represent constrictions in the hair shafts at irregular intervals. Repeated formation of these Pohl-Pinkus constrictions (PPC) during the course of disease activity results in the formation of monilethrix-like hairs. In our study, PPC was observed in one patient and Mane et al. [10] reported in two of his patients.

Correlation between dermoscopic features and disease activity

In the present study, disease activity assessed by hair pull test of each patch correlated positively with BD, BH, and TH. SVH correlated negatively with the disease activity, but this was not statistically significant. Positive correlation was observed earlier [7] and the present study further confirms that. Peter et al. [13] did not find any correlation with the disease activity. Positive correlation in the present study with BD, BH, and TH can be explained on the basis that they represent distinct but similar ways, in which the hair follicle responds to an initial inflammatory insult at the hair bulb region. Initially, a constriction (PPC) occurs in the mid part of the proximal hair shaft, later proximal end of these hairs becomes thinner than the distal end (CH). Sometimes, CH may regain normal thickness with cessation of an inflammatory insult, or these hairs may eventually break resulting in BH or TH, and if the inflammatory insult is continuous, hair shafts become progressively thinner and break at the level of scalp to form a BD. Thus, BD, BH, and TH are the result of most severely affected follicles, whereas CH and PPC are the result of least severely affected follicles. Absence of correlation between CH and PPC and the disease activity in the present study might be due to the fact that they represent the least severely affected hairs. Moreover, in the present study, these markers of disease activity (BD and BH) were found in 20% of clinically inactive patches (negative hair pull test). Thus, dermoscopy was more sensitive in recognizing the active patches than the subjective hair pull test.

Correlation between dermoscopic features and the disease severity

Similar to most of the earlier studies, our study did not find any significant correlation between any of the dermoscopic features and the severity of AA (assessed by SALT score). [10],[13] However, in Inui et al.[7] study, BD and YD correlated positively and SVH negatively with severity of AA. This can be explained on the basis that the SALT score, which is the percentage of terminal hair loss in each of the four views of scalp may include active, stable, and regressing lesions. One such dermoscopic pattern may not be significant in such a mixture of lesions with different activities.

Conclusion

The most common dermoscopic pattern in our study was YD. Micro-exclamation mark hairs are a marker of disease activity can be demonstrable only with the help of dermoscopy. Presence of BDs, BHs, and THs strongly indicate active disease in the patch. These dermoscopic signs of disease activity were seen in some clinically inactive patches in our study, thus helping us to pick up more active patches which were not identified clinically or by positive hair pull test, thus enabling active intervention at an earlier date.

What is new?
Micro-exclamation mark hairs are a marker of disease activity can be demonstrable only with the help of dermoscopy. Presence of black dots, broken hair, and tapering hair indicate active disease.